Magnetic Source Imaging and Infant MEG: Current Trends and Technical Advances

Magnetoencephalography (MEG) is known for its temporal precision and good spatial resolution in cognitive brain research. Nonetheless, it is still rarely used in developmental research, and its role in developmental cognitive neuroscience is not adequately addressed. The current review focuses on the source analysis of MEG measurement and its potential to answer critical questions on neural activation origins and patterns underlying infants’ early cognitive experience. The advantages of MEG source localization are discussed in comparison with functional magnetic resonance imaging (fMRI) and functional near-infrared spectroscopy (fNIRS), two leading imaging tools for studying cognition across age. Challenges of the current MEG experimental protocols are highlighted, including measurement and data processing, which could potentially be resolved by developing and improving both software and hardware. A selection of infant MEG research in auditory, speech, vision, motor, sleep, cross-modality, and clinical application is then summarized and discussed with a focus on the source localization analyses. Based on the literature review and the advancements of the infant MEG systems and source analysis software, typical practices of infant MEG data collection and analysis are summarized as the basis for future developmental cognitive research.

[1]  E. Halgren,et al.  Dynamic Statistical Parametric Mapping Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000, Neuron.

[2]  Jukka Sarvas,et al.  Brain Signals: Physics and Mathematics of MEG and EEG , 2019 .

[3]  R. T. Wakai,et al.  Development of MEG sleep patterns and magnetic auditory evoked responses during early infancy , 2006, Clinical Neurophysiology.

[4]  H. Otsubo,et al.  Total intravenous anesthesia affecting spike sources of magnetoencephalography in pediatric epilepsy patients: Focal seizures vs. non-focal seizures , 2013, Epilepsy Research.

[5]  Donald C. Rojas,et al.  Children and Adolescents with Autism Exhibit Reduced MEG Steady-State Gamma Responses , 2007, Biological Psychiatry.

[6]  Luke Bloy,et al.  The maturation of auditory responses in infants and young children: a cross-sectional study from 6 to 59 months , 2015, Front. Neuroanat..

[7]  Z J Koles,et al.  EEG source localization: implementing the spatio-temporal decomposition approach. , 1998, Electroencephalography and clinical neurophysiology.

[8]  Hubert Preissl,et al.  Development of auditory evoked fields in human fetuses and newborns: A longitudinal MEG study , 2005, Clinical Neurophysiology.

[9]  Rachel Marsh,et al.  Reduced functional connectivity within the limbic cortico‐striato‐thalamo‐cortical loop in unmedicated adults with obsessive‐compulsive disorder , 2014, Human brain mapping.

[10]  Susan Bowyer,et al.  Cervical Dystonia and Executive Function: A Pilot Magnetoencephalography Study , 2018, Brain sciences.

[11]  Kevin Pratt,et al.  BabySQUID: A mobile, high-resolution multichannel magnetoencephalography system for neonatal brain assessment , 2006 .

[12]  Toshiaki Imada,et al.  Magnetoencephalography is feasible for infant assessment of auditory discrimination , 2004, Experimental Neurology.

[13]  Niall Holmes,et al.  Moving magnetoencephalography towards real-world applications with a wearable system , 2018, Nature.

[14]  V. Litvak,et al.  Cortico-subthalamic Coherence in a Patient With Dystonia Induced by Chorea-Acanthocytosis: A Case Report , 2019, Front. Hum. Neurosci..

[15]  Hari Eswaran,et al.  Spontaneous neuronal activity in fetuses and newborns , 2004, Experimental Neurology.

[16]  T. Brown,et al.  Variability of magnetoencephalographic sensor sensitivity measures as a function of age, brain volume and cortical area , 2014, Clinical Neurophysiology.

[17]  Hubert Preissl,et al.  Neuromagnetic signatures of syllable processing in fetuses and infants provide no evidence for habituation. , 2016, Early human development.

[18]  Silvia Comani,et al.  The intrahemispheric functional properties of the developing sensorimotor cortex are influenced by maturation , 2015, Front. Hum. Neurosci..

[19]  Eric Halgren,et al.  Spatiotemporal neural dynamics of word understanding in 12- to 18-month-old-infants. , 2011, Cerebral cortex.

[20]  Zhi-jun Zhang,et al.  Resting brain connectivity: changes during the progress of Alzheimer disease. , 2010, Radiology.

[21]  R. Wakai,et al.  Improved neuromagnetic detection of fetal and neonatal auditory evoked responses , 2001, Clinical Neurophysiology.

[22]  Rui Yan,et al.  Identification of major depressive disorder and prediction of treatment response using functional connectivity between the prefrontal cortices and subgenual anterior cingulate: A real-world study. , 2019, Journal of affective disorders.

[23]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[24]  Hubert Preissl,et al.  Magnetoencephalographic Signatures of Numerosity Discrimination in Fetuses and Neonates , 2014, Developmental neuropsychology.

[25]  Martin Luessi,et al.  MNE software for processing MEG and EEG data , 2014, NeuroImage.

[26]  J. Hirsch,et al.  The present and future use of functional near‐infrared spectroscopy (fNIRS) for cognitive neuroscience , 2018, Annals of the New York Academy of Sciences.

[27]  Seppo P. Ahlfors,et al.  Head movements of children in MEG: Quantification, effects on source estimation, and compensation , 2008, NeuroImage.

[28]  Mitsuru Kikuchi,et al.  Developmental Trajectory of Infant Brain Signal Variability: A Longitudinal Pilot Study , 2018, Front. Neurosci..

[29]  A. Nobre,et al.  Magnetoencephalography , 1990, The Lancet.

[30]  R. Wakai,et al.  Fetal auditory evoked responses detected by magnetoencephalography. , 1996, American journal of obstetrics and gynecology.

[31]  Timothy P. L. Roberts,et al.  Magnetoencephalography and the infant brain , 2019, NeuroImage.

[32]  Yong He,et al.  Assessment of system dysfunction in the brain through MRI-based connectomics , 2013, The Lancet Neurology.

[33]  Elina Pihko,et al.  Development of Human Somatosensory Cortical Functions – What have We Learned from Magnetoencephalography: A Review , 2014, Front. Hum. Neurosci..

[34]  Christian O'Reilly,et al.  Is functional brain connectivity atypical in autism? A systematic review of EEG and MEG studies , 2017, PloS one.

[35]  M. Funke,et al.  Magnetoencephalographic Recordings in Infants: A Retrospective Analysis of Seizure-Focus Yield and Postsurgical Outcomes , 2018, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[36]  John E Richards,et al.  Cortical Source Localization of Infant Cognition , 2009, Developmental neuropsychology.

[37]  Toshiaki Imada,et al.  Infants’ brain responses to speech suggest Analysis by Synthesis , 2014, Proceedings of the National Academy of Sciences.

[38]  D. Cohen Magnetoencephalography: Evidence of Magnetic Fields Produced by Alpha-Rhythm Currents , 1968, Science.

[39]  M. Molteni,et al.  Building Blocks of Others' Understanding: A Perspective Shift in Investigating Social-Communicative Deficit in Autism , 2016, Front. Hum. Neurosci..

[40]  P. Kuhl,et al.  Musical intervention enhances infants’ neural processing of temporal structure in music and speech , 2016, Proceedings of the National Academy of Sciences.

[41]  P. Kuhl,et al.  Infant speech perception activates Broca's area: a developmental magnetoencephalography study , 2006, Neuroreport.

[42]  S. Kärkkäinen,et al.  Left hemisphere enhancement of auditory activation in language impaired children , 2019, Scientific Reports.

[43]  Samu Taulu,et al.  The Importance of Properly Compensating for Head Movements During MEG Acquisition Across Different Age Groups , 2016, Brain Topography.

[44]  M. Berchicci,et al.  Development of Mu Rhythm in Infants and Preschool Children , 2011, Developmental Neuroscience.

[45]  G. A. Miller,et al.  Interpreting abnormality: an EEG and MEG study of P50 and the auditory paired-stimulus paradigm , 2003, Biological Psychology.

[46]  Richard N Aslin,et al.  Questioning the questions that have been asked about the infant brain using near-infrared spectroscopy , 2012, Cognitive neuropsychology.

[47]  R. Wakai,et al.  Slow rhythms and sleep spindles in early infancy , 2016, Neuroscience Letters.

[48]  R T Wakai,et al.  MEG sleep pattern dependence of auditory evoked fields in young infants. , 2004, Neurology & clinical neurophysiology : NCN.

[49]  Karl J. Friston,et al.  Oscillatory, Computational, and Behavioral Evidence for Impaired GABAergic Inhibition in Schizophrenia , 2019, Schizophrenia bulletin.

[50]  Hubert Preissl,et al.  Auditory habituation in the fetus and neonate: an fMEG study. , 2013, Developmental science.

[51]  Dinggang Shen,et al.  The UNC/UMN Baby Connectome Project (BCP): An overview of the study design and protocol development , 2019, NeuroImage.

[52]  Risto Näätänen,et al.  Speech-sound discrimination in neonates as measured with MEG , 2004, Neuroreport.

[53]  R. Näätänen,et al.  Auditory magnetic responses of healthy newborns , 2003, Neuroreport.

[54]  Sylvain Baillet,et al.  Magnetoencephalography for brain electrophysiology and imaging , 2017, Nature Neuroscience.

[55]  Aina Puce,et al.  A Review of Issues Related to Data Acquisition and Analysis in EEG/MEG Studies , 2017, Brain sciences.

[56]  Riitta Salmelin,et al.  Magnetoencephalography: From SQUIDs to neuroscience Neuroimage 20th Anniversary Special Edition , 2012, NeuroImage.

[57]  Bethany Routley,et al.  Reliability of Static and Dynamic Network Metrics in the Resting-State: A MEG-Beamformed Connectivity Analysis , 2018, bioRxiv.

[58]  Andrew C. Papanicolaou,et al.  Clinical Magnetoencephalography and Magnetic Source Imaging: The method , 2009 .

[59]  H. Preissl,et al.  Fetal magnetoencephalography: viewing the developing brain in utero. , 2005, International review of neurobiology.

[60]  Ruth A. Carper,et al.  Autism and Abnormal Development of Brain Connectivity , 2004, The Journal of Neuroscience.

[61]  S Taulu,et al.  MEG recordings of DC fields using the signal space separation method (SSS). , 2004, Neurology & clinical neurophysiology : NCN.

[62]  J. Burneo,et al.  A systematic review on MEG and its use in the presurgical evaluation of localization-related epilepsy , 2008, Epilepsy Research.

[63]  E. Pihko,et al.  Increasing the efficiency of neonatal MEG measurements by alternating auditory and tactile stimulation , 2011, Clinical Neurophysiology.

[64]  V. Calhoun,et al.  Relationship between MEG global dynamic functional network connectivity measures and symptoms in schizophrenia , 2018, Schizophrenia Research.

[65]  Yoshio Okada,et al.  Somatosensory evoked potentials and magnetic fields elicited by tactile stimulation of the hand during active and quiet sleep in newborns , 2004, Clinical Neurophysiology.

[66]  Lutz Trahms,et al.  Optically Pumped Magnetometers for MEG , 2019, Magnetoencephalography.

[67]  Yoshio Okada,et al.  Somatosensory evoked magnetic fields to median nerve stimulation in newborns , 2005 .

[68]  M. Kikuchi,et al.  Magnetoencephalography in the study of children with autism spectrum disorder , 2016, Psychiatry and clinical neurosciences.

[69]  P. Sarzi-Puttini,et al.  Evaluation of salivary and plasma microRNA expression in patients with Sjögren's syndrome, and correlations with clinical and ultrasonographic outcomes. , 2019, Clinical and experimental rheumatology.

[70]  Hubert Preissl,et al.  Sensitivity to Auditory Spectral Width in the Fetus and Infant – An fMEG Study , 2013, Front. Hum. Neurosci..

[71]  Christoph Pfeiffer,et al.  Evaluation of realistic layouts for next generation on-scalp MEG: spatial information density maps , 2017, Scientific Reports.

[72]  Selma Supek,et al.  Magnetoencephalography: From Signals to Dynamic Cortical Networks , 2014 .

[73]  Viktor Klüber,et al.  MNE Scan: Software for real-time processing of electrophysiological data , 2018, Journal of Neuroscience Methods.

[74]  F. D. Silva,et al.  EEG and MEG: Relevance to Neuroscience , 2013, Neuron.

[75]  Moriah E. Thomason,et al.  Functional plasticity before the cradle: A review of neural functional imaging in the human fetus , 2013, Neuroscience & Biobehavioral Reviews.

[76]  M. Asada,et al.  Hyperscanning MEG for understanding mother–child cerebral interactions , 2014, Front. Hum. Neurosci..

[77]  S Tobimatsu,et al.  A magnetoencephalographic study on development of the somatosensory cortex in infants , 2001, Neuroreport.

[78]  Hubert Preissl,et al.  Sound frequency change detection in fetuses and newborns, a magnetoencephalographic study , 2005, NeuroImage.

[79]  E. Pihko,et al.  Magnetoencephalography in neonatology , 2012, Neurophysiologie Clinique/Clinical Neurophysiology.

[80]  Yoshio Okada,et al.  Cortical Somatosensory Reorganization in Children with Spastic Cerebral Palsy: A Multimodal Neuroimaging Study , 2014, Front. Hum. Neurosci..

[81]  Joni N. Saby,et al.  Infant brain responses to felt and observed touch of hands and feet: an MEG study. , 2018, Developmental science.

[82]  Adrian K. C. Lee,et al.  Potential Use of MEG to Understand Abnormalities in Auditory Function in Clinical Populations , 2014, Front. Hum. Neurosci..

[83]  Amy L. Proskovec,et al.  Neuroimaging with magnetoencephalography: A dynamic view of brain pathophysiology. , 2016, Translational research : the journal of laboratory and clinical medicine.

[84]  Luke Bloy,et al.  Artemis 123: development of a whole-head infant and young child MEG system , 2014, Front. Hum. Neurosci..

[85]  Blake W. Johnson,et al.  Measurement of brain function in pre-school children using a custom sized whole-head MEG sensor array , 2010, Clinical Neurophysiology.

[86]  Hubert Preissl,et al.  Neonatal and fetal response decrement of evoked responses: A MEG study , 2008, Clinical Neurophysiology.

[87]  Yoshio Okada,et al.  Immaturity of somatosensory cortical processing in human newborns , 2006, NeuroImage.

[88]  Minna Huotilainen,et al.  Using magnetoencephalography in assessing auditory skills in infants and children. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[89]  R. Burgess,et al.  Magnetoencephalographic Recordings in Infants Using a Standard-Sized Array: Technical Adequacy and Diagnostic Yield , 2017, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[90]  Eric Larson,et al.  Mapping cortical dynamics using simultaneous MEG/EEG and anatomically-constrained minimum-norm estimates: an auditory attention example. , 2012, Journal of visualized experiments : JoVE.

[91]  Yoshio Okada,et al.  Evoked magnetic fields from primary and secondary somatosensory cortices: A reliable tool for assessment of cortical processing in the neonatal period , 2012, Clinical Neurophysiology.

[92]  Minna Huotilainen,et al.  Newborns discriminate novel from harmonic sounds: A study using magnetoencephalography , 2006, Clinical Neurophysiology.

[93]  Peter C. Hansen,et al.  MEG. An introduction to methods , 2010 .

[94]  Yoshio Okada,et al.  Somatosensory evoked magnetic fields from the primary and secondary somatosensory cortices in healthy newborns , 2008, NeuroImage.

[95]  N Jon Shah,et al.  Ocular and cardiac artifact rejection for real-time analysis in MEG , 2014, Journal of Neuroscience Methods.

[96]  Hubert Preissl,et al.  Serial magnetoencephalographic study of fetal and newborn auditory discriminative evoked responses. , 2007, Early human development.

[97]  J. Stephen,et al.  Maturation of somatosensory cortical processing from birth to adulthood revealed by magnetoencephalography , 2009, Clinical Neurophysiology.

[98]  Minna Huotilainen,et al.  Change detection in newborns using a multiple deviant paradigm: A study using magnetoencephalography , 2009, Clinical Neurophysiology.

[99]  Stephen E. Jones,et al.  Magnetoencephalographic Identification of Epileptic Focus in Children With Generalized Electroencephalographic (EEG) Features but Focal Imaging Abnormalities , 2017, Journal of child neurology.

[100]  R. Schultz,et al.  Resting-State Alpha in Autism Spectrum Disorder and Alpha Associations with Thalamic Volume , 2015, Journal of autism and developmental disorders.

[101]  Hubert Preissl,et al.  Magnetoencephalography in healthy neonates , 2006, Clinical Neurophysiology.

[102]  K. McNally,et al.  Preoperative evaluation and surgical management of infants and toddlers with drug-resistant epilepsy. , 2018, Neurosurgical focus.

[103]  Jed A. Meltzer,et al.  Spontaneous oscillatory markers of cognitive status in two forms of dementia , 2018, Human brain mapping.

[104]  Toshiaki Imada,et al.  Theta brain rhythms index perceptual narrowing in infant speech perception , 2013, Front. Psychol..

[105]  Hubert Preissl,et al.  Developmental Cognitive Neuroscience Habituation of Visual Evoked Responses in Neonates and Fetuses: a Meg Study , 2022 .

[106]  P. Ellen Grant,et al.  Effects of sutures and fontanels on MEG and EEG source analysis in a realistic infant head model , 2013, NeuroImage.

[107]  Eugen Trinka,et al.  Magnetoencephalography (MEG): Past, current and future perspectives for improved differentiation and treatment of epilepsies , 2017, Seizure.

[108]  Samu Taulu,et al.  Speech discrimination in 11-month-old bilingual and monolingual infants: a magnetoencephalography study. , 2017, Developmental science.

[109]  A. Goldstein,et al.  Brain responses to other people's pain in fibromyalgia: a magnetoencephalography study. , 2019, Clinical and experimental rheumatology.

[110]  Hubert Preissl,et al.  Early development of brain responses to rapidly presented auditory stimulation: A magnetoencephalographic study , 2010, Brain and Development.

[111]  Zhong-Lin Lu,et al.  Magnetic source imaging of the human brain , 1993, Photonics West - Lasers and Applications in Science and Engineering.

[112]  Lisa Blaskey,et al.  MEG detection of delayed auditory evoked responses in autism spectrum disorders: towards an imaging biomarker for autism , 2010, Autism research : official journal of the International Society for Autism Research.

[113]  Paavo Alku,et al.  Sleeping newborns extract prosody from continuous speech , 2008, Clinical Neurophysiology.

[114]  P. Ellen Grant,et al.  Exploring early human brain development with structural and physiological neuroimaging , 2019, NeuroImage.

[115]  Vince Daniel Calhoun,et al.  Dynamic Functional Network Connectivity in Schizophrenia with Magnetoencephalography and Functional Magnetic Resonance Imaging: Do Different Timescales Tell a Different Story? , 2019, Brain Connect..

[116]  H. Preissl,et al.  Impact of Intrauterine Growth Restriction on Cognitive and Motor Development at 2 Years of Age , 2018, Front. Physiol..